Arbuscular Mycorrhizas Alleviate Plant Stress: Analysis of

1 Department of Physics, Federal University of Minas Gerais, Belo Horizonte, MinasGerais, Brazil.

2 Instituto Spegazzini, Av 53 No 477, B1900AVJ La Plata, Argentina* Corresponding author: E-mail: [email protected]

8

Arbuscular Mycorrhizas Alleviate Plant Stress:Analysis of Studies from South America

MARCELA CLAUDIA PAGANO1* AND MARTA NOEMÍ CABELLO2

ABSTRACT

Interest in stressful conditions is rising with increasing the recognitionthat global changes can negatively affect plant diversity and ecosystemfunction. It is known that arbuscular mycorrhizas (AM) permit the plantto perform better under stressful and unfavorable conditions, recruitingtheir symbiont in the soil. Recent reports on plant growth under differentlevels of stress and AM account for 94% of the published papers on AM.Stress affects soil physical and chemical properties, influencing thepopulation, diversity and activities of soil microbes, including symbioticfungal populations. This review was done to explore the currentinformation on the benefits of AM symbioses in stressed systems, withrespect to the research results in South America. The increasingappreciation that in-arid regions most trees are mycorrhizal has alsodeep consequences for rehabilitation efforts of woodlands and forestshowing that underground processes are crucial for understanding ofecosystem function.Thus, relevant findings related to the benefits of AMmanagement by increasing stress tolerance are emphasized. Accordingly,research paths that are necessary for the increased understating of

132 Biotechnological Techniques of Stress Tolerance in Plants

mycorrhizal benefits under stress conditions, which deserve increasingattention are discussed.

Key words: Arbuscular mycorrhizas, Plant stress, Soil stress, SouthAmerica

INTRODUCTION

Interest in stressful conditions is rising with increasing the recognitionthat global changes can negatively affect ecosystem diversity andfunction (Firbank et al., 2008, Scherr and McNeely, 2008). It is knownthat the environment affect organism in many ways calledenvironmental factors (see Table 1), which can be biotic or abiotic.Interactions with other organisms (biotic environmental factors) areinfection or damage by herbivory or trampling and also symbioses andparasitism. Other interesting biotic factors are allelochemicals(originally defined as secondary metabolites involved in plant-plant andplant-microorganism interactions), and nowadays considered naturalproduct playing a role in plant-environment interactions (Leicach etal. 2009). For example, eucalypts are considered one of the mostnotorious allelophatic trees (El-Khawas and Shehata, 2005).

Table 1: Main plant stress factors. Adapted from Schulze et al. (2002)

Type

Biotic InfectionHerbivory (damage or trampling)Competition

Abiotic Temperature HeatCold Chilling

Frost

Water DroughtFlooding

Radiation LightUVIonizing radiation

Chemical stress Mineral salts Deficiency, over-supplypH, salinity

Pollutants Heavy metalsPesticides

Gaseous toxins

Mechanical stress WindSoil movementSubmergence

133Arbuscular Mycorrhizas Alleviate Plant Stress

The effect of abiotic environmental factors (temperature, humidity,light, water supply, nutrients, and CO2) varied with their intensity anddetermine plant growth (Schulze et al., 2002). Moreover, wind orpollutants are also abiotic factors, the latest of increasingly researchnowadays. It is known that plant tolerances to abiotic stresses suchas drought, cold, and salinity have been reported for different plantspecies, such as eucalypts. Stress can be used on a scale of intensity(from deficiency to excessive supply), thus the environmental factorsbecome stress factors (Schulze et al., 2002).

As plants are sessile organisms exposed to natural climatic or edaphicstresses (drought, high irradiation, heat, frost, flooding, nutrientdifferences) and to environmental changes from human activities (airand soil pollution, soil degradation, etc.) (Schützendübel and Polle, 2002)biotechnological techniques of stress tolerance in plants are increasinglysought. For example, under stress arbuscular mycorrhizal fungi (AMF)are able to modify plant physiology in a way to cope with thoseenvironmental factors (Miransari et al., 2008). Several reports haveshowed that mycorrhizal symbiosis improves plant health throughincreased protection against environmental stresses, either biotic (e.g.,pathogen attack) or abiotic (e.g., drought, salinity, heavy metals, organicpollutants) (Azcón and Barea, 2010; Barea et al., 2005a,b).

It is known that abiotic stresses adversely affect plant growth,productivity and trigger morphological, physiological, biochemical andmolecular changes in plants. For example, cold stress limits theagricultural productivity of plants in hilly areas.

Mineral salts deficiency are usually recomposed by using commercialfertilizers (labeled with a formula that indicates the percentage of eachelement, e.g., 04-30-10 NPK fertilizer contains 4% N, 30% P and 5%K). Additionally, some micronutrients (iron, sulfur, magnesium, zinc,and boron) are incorporated to soil as they can sometimes becomelimiting factors (Raven et al., 2005). New directions in microbial ecologyhave need of integration of microbial physiological ecology, populationbiology, and process ecology as microorganisms have a diversity ofevolutionary adaptations and physiological mechanisms to copeenvironmental stress (Schimel et al., 2007).

Nevertheless, little attention has been paid to soil stresses and theireffect in roots. For example, tillage promote disruption of the AMFhyphal network and dilution of the propagule-rich in topsoil (Schalamukand Cabello, 2010) and affects the soil physical and chemical properties,modifying the number, diversity and activity of the soil microflora,


including both free and symbiotic fungal populations (Pagano, 2011).In this sense, AMF enhances soil structure through the formation ofhydro-stable aggregates necessary for good soil tilth (Rillig andMummey, 2006; Ruíz-Lozano et al., 2008).

AMF can improve plant growth and production under differentconditions, including various soil stresses (reviewed by Miransari 2010).It is known that heavy metals, compaction, drought and salinity candecrease plant growth and production. However, AMF can promote plantgrowth increasing plant production under stress due to their benefits:establishment of extensive hyphal networks and secretion ofbiochemicals like glomalin, which enhance water and nutrient uptakemeliorating soil structure (reviewed by Miransari, 2010).

It is interesting to mention that Biotechnology offers new strategiesthat can be used to develop transgenic crop plants with improvedtolerance to stresses. Moreover, germplasm collected from high altitudeand low temperature areas, cold tolerant mutant, and wild species canbe exploited for improved tolerant genotypes in other areas. Then, theimpacts of two important plant stressors, drought and freezing, onmicrobial and plant physiology will be also addressed here.

Lastly, biochar soil amendment not only can contribute to improvedsoil fertility and plant productivity, but can benefit microorganismpopulations that promote plant growth and resistance to biotic stresses(soil borne diseases and foliar pathogens). The mechanisms by whichit is benefic are scarcely understood, and indirect effects (increasedwater and nutrient retention, improvements in soil pH, increased soilcation exchange capacity, effects on P and S transformations andturnover, neutralization of phytotoxic compounds in the soil, improvedsoil physical properties, and alteration of soil microbiota (Elad et al.,2011). Interestingly, biochar promote AMF and in this regard, furtherstudies are needed (Warnock et al., 2007).

This chapter examines the current information on the benefits ofAM symbioses in stressed plant systems, with respect to the researchresults in South America. Additionally, soil amendments that may havea synergistic influence are discussed.

ARBUSCULAR MYCORRHIZAL FUNGI AND PLANTS

Plants provide several services (provisioning of plant products, erosioncontrol, invasion resistance, pathogen and pest regulation and soil


fertility regulation)(Quijas et al., 2010). The vegetation cover is the mostimportant vegetation parameter for soil erosion (interrill or rill erosion)control as well as the influence of plant roots is increasingly studiedin this sense (e.g. for rill and ephemeral gully erosion) (Gyssels et al.,2005).

Additionally, plants interact with below-ground group ofmicroorganisms (Kuyper and Goede, 2005) as well as above-ground(Zheng and Dicke, 2008).

For example, the numbers of worldwide species of rhizobia (98 speciesin 13 genera) (http://www.rhizobia.co.nz/) and of AMF (230 species in13 genera) (www.mycobank.org) is much lower than that of legumes(18,000) or AM plants (3,617 species in 263 families) (Wang and Qiu,2006), totaling more than 3,941 [over 324 AM plant species compiledby Pagano (2012)] and estimated in 200,000 (Kuyper and Goede, 2005).

To know the mycotrophic status in plant species is an importanttool for various purposes such as seedling production, plant cultivation(greenhouse or field), ecological restoration, endangered speciesprotection, to differentiate plant functional types and for screening forplant stress tolerance. Information on parasitic AMF association is alsoneeded.

It is known that parasitic interactions show a larger degree ofselectivity of species than mutualisms; but selectivity is also the rulein the last associations, mostly at lower taxonomic level (Kuyper andGoede, 2005).

Little is known about the perception of abiotic stress by plants atthe molecular level (Schulze et al., 2002). However, mycorrhizosphereconditions are part of the common plant-microbe strategies and plant-defending mechanisms that can result in a better stress-alleviation atchronic metal-exposures (Biró et al., 2012), for example. There aresignaling compounds produced by the host plant to promote rootcolonization by AMF such as strigolactones (Bouwmeester et al., 2007).It is also known that isoprenoids and Jasmonic acid (JA) play a rolein plant defense protection, which is related to the establishments andfunctionality of mycorrhizal symbiosis (Pozo and Azcón-Aguilar, 2007).

The AMF symbiosis can potentiate C allocation to root exudates andgive more resources to plant, to synthesize essential isoprenoids andto use them for its growth. The JA application might contribute to theshoot response to root colonization by AM fungi (Isayenkov et al., 2005)


with potential enhance of defense status (Augé, 2001; Cordier et al.,1998; Hause and Schaarschmidt, 2009; Asensio et al., 2012).

Thus, increasing experiments worldwide are subjecting the plantsto stressors such as drought and to exogenous application of planthormones or pesticides, in order to test the interaction between AMsymbiosis, biochar and plants.

Since the publication of the seminal books of Sieverding (1991), Smithand Read (2008), van der Heijden and Sanders (2003) and Miransariet al. (2008) and several reports (see Table 2) it was highlighted theneed for more information on how AMF influence plant stress indifferent crop species. However, to increase our ability to optimizemanagement of AMF in field situations is still urgently needed.

Table 2: Some recent book and reports dealing with occurrence of AMF in stressedconditions

Reports on AMF and plant stress Biome/ ecosystems/ Referencescountry

AMF in native species and soil/ Cerrado, Brazil Detmann et al. (2008)climatic stress

AMF in Calolisianthus species/ Rupestrian field, Brazil Delgado et al. (2011)water deficit and nutritional stress

Mycorrhizal biotechnology, AMF, Several ecosystems Tangaduraiphytoremediation, climatic changes et al. (2010)

AMF and soil stresses Several ecosystems Miransari (2010)

AMFand heavy metals stress, Brazil Cabral et al. (2010);phytoextraction greenhouse Silva et al. (2006)experiments

Drought tolerance and AMF in Grassland, Argentina Busso et al. (2008)three perennial grasses

AMF and alleviation of soil stresses Several ecosystems Miransari et al. (2008)

AMF and alleviation of soil stresses Several ecosystems Siddiqui et al. (2008)

AMF and soil and environmental Several ecosystems Smith and Read (2008)stresses

AMF and hydrocarbon soil stress Polluted soils Cabello (2001)Argentina and Germany

ARBUSCULAR MYCORRHIZAL PLANTS AND DROUGHT STRESS

Of serious significance are the effects of global change on soils: increasedsoil temperatures, increased nutrient availability, increased groundinstability in mountainous regions, and increased erosion from floods.


As nutrient and water limitations increase, plants can allocate morephotosynthate to mycorrhizal hyphae to increase soil resource uptake,which can be seen particularly in high latitude and high altitudeecosystems (See Simard and Austin, 2010).

Plant responses to water deficiency are complex (and include stressavoidance or tolerance). It is known that stomata close in response towater deficit; however, it is more related to soil moisture than to leafwater status, involving chemical signals produced by roots (Chaveset al., 2002).

Mycorrhizal plants under drought conditions increase stomatalconductance, transpiration rate and leaf water potential due to a higherwater uptake (Augé, 2001) than non-mycorrhizal plants. However, themechanism by which the fungus modifies host-plant water relationsremains unknown (different hypotheses have been tested withinconclusive results (Morte et al., 2000) and the contribution of AMsymbiosis to plant drought tolerance is nowadays seen as the resultof accumulative effects (physical, nutritional, physiological and cellular)(Ruiz-Lozano, 2003).

In 2009, Monroy Ata and Sánchez compiled the benefits of AMF insemiarid plants of Mexico. They showed better water relations and plantgrowth in such environments in comparison with uninoculated controlplants.

Recently, Barea et al. (2011) compiled the diversity of mycorrhizasfound in semiarid Mediterranean ecosystem in SE Spain. They showedthe benefit of mycorrhizal fungi to help plants to establish and dealwith nutrient deficiency, drought, soil disturbance and otherenvironmental stresses characteristically involved in soil degradation.

In Brazil, reports from highland fields from deciduous forest (SeePagano and Araújo, 2011; Pagano, 2012) pointed out a total of ~28 AMplant species and at least 36 AM species that occurs in those ecosystems(Pagano et al., 2013). Additionally, Carvalho et al. (2012) reported 49AMF species in highland fieldsfrom Minas Gerais State, Brazil, of them23 AMF species are in common with the reports cited above.

Argentinean arid and semiarid regions present in general xerophyticplants, forming dry forests, open scrublands, shrub steppe, etc. Lugoet al. (2002, 2008) studied different vegetal types such as Jarillal andPuna vegetation and compiled information on mycorrhizal status of225 AM plant species (see Pagano et al., 2012), some of them also


associate with dark septate endophitic fungi (DSE). In dry Punaecosystem (2000 to 4400 m. a. s. l.) ten AMF species were found, andGlomus was the predominant genus.

ARBUSCULAR MYCORRHIZAL PLANTS AND FLOODING STRESS

Flooding has proved to be a usual stress affecting agriculture andforestry, being able to change soil microbial abundances, includingrhizobial composition as seen in experiments of land restoration in theRio Doce valley, Minas Gerais, Brazil (Pagano, 2008). The tropicallegume tree (Centrolobium tomentosum) tested for functional andstructural riparian restoration showed renodulation by fast-growingstrains after flood disturbance (plants were inoculated with a fast growthRhizobium strain) than uninoculated plants.

In general, less research has been focused on conditions of excesswater, although some aquatic and wetland plants associate with AMF(see Pagano 2012). The function of AM fungi in Florida wetland, forexample, do not appeared to be restricted by hydroperiod. Rootcolonization is probable controlled by plant factors such as carbonavailability (Ipsilantis and Sylvia, 2007).

Using phylogenetic analysis, Wang et al. (2011) also showed thatflooding plays an important role in AMF diversity, and its effects appearto depend on the degree (duration) of flooding. Both host species andtide level affected community structure of AMF, indicating the presenceof habitat and host species preferences (Wang et al., 2011). Additionally,Radhika et al. (2012) showed the benefits of AM association inmangroves from Ganges river, India, to cope soil physical and chemicalstress.

In the Argentinean flooding pampa the mycorrhizal colonization ofthe community of Paspalum dilatatum (a highly palatable, dominantspecies) was higher in the continuous grazing plots (Grigera andOesterheld, 2004) than in exclosure sites.

ENVIRONMENTAL STRESS FROM HUMAN ACTIVITIES

Arbuscular Mycorrhizal Fungi and Tillage

Anthropogenic alterations to improve the productivity of field crops(e.g. tillage, monoculture, crop rotation, irrigation, amendments and


crop protection) can be denominated as perturbation stresses, resultin disturbance of the native soil microbial ecosystem. While moderateperturbation will be benefic in the short term, higher levels of stressmay result in degraded soils (Sturz and Christie, 2003).

Nowadays, the conventional tillage system is still commonly usedin most countries, usually consisting in the use of moldboard plowingand additional secondary operations to prepare the seedbed. However,field traffic or intensive tillage result in excessive soil compaction andsoil water loss.

It is known that tillage reduce AMF spore and hyphal lengthdensities, as well as decreased glomal in concentrations in bothtemperate and tropical soils (Wright et al., 1999; Boddington and Dodd,2000). The composition and diversity of AMF spore communities wereaffected by tillage in a number of studies (Pagano, 2011). Moreover,direct effects of tillage on AMF propagules are the following: thedisruption of the hyphal network; the dilution of the propagule-richtopsoil; and accelerated root decomposition (Schalamuk and Cabello,2010).

In addition, AM fungi can be strongly decreased by conventionalagricultural practices, possibly due to disturbance of AM fungal hyphalnetworks, changes in soil nutrient content, altered microbial activity,or changes in weed populations (Jansa et al., 2003; 2006).

In Argentina, earlier studies have found less management of AMFin order to increase plant productivity (Covacevich and Echeverria,2009). Soils of the Pampas region present high native AMF that colonizecrop plants under different management systems (Covacevich et al.,2006; 2007, Schalamuk et al., 2006; Covacevich et al., 2008); however,they are not yet manipulated.

More recently, Schalamuk and Cabello (2010) showed that differenttypes of AM inocula from a field experiment with tilled and no-tilledwheat and from nondisturbed treatments (spontaneous vegetation),presented different proportions of AM families (Acaulosporaceae,Gigasporaceae, Glomeraceae), between field and trap cultures.Glomeraceae were higher in the trap cultures, which was attributedto the use of intra- and/or extra radical mycelium, showing advantagesin the use of these propagules.


ARBUSCULAR MYCORRHIZAL FUNGI AND PLANT BIOTICSTRESSES

Biotic stresses (disease, herbivory and/or the presence of competitors)as much as abiotic stresses such as nutrient deficiency and droughtcan affect both plant and simbiont fitness. Damage caused by bioticfactors such as herbivory have often enhance secondary metabolism,however response depends on the particular species. It is known thatmany plants species respond to herbivory or pathogens attack byincreasing synthesis and releasing jasmonic acid and methyl jasmonate,starting in damaged organs.

With regard to AMF symbioses, Wehner et al. (2010) indicate themechanisms of protection of host plants from root pathogenic fungi bydifferent AMF species. They pointed out the little evidence and thefocus on Glomus species, such as Glomus intraradices and Funneliformesmosseae, which do not represent of the whole fungal biodiversity. Onlyone report (Maherali and Klironomos, 2007) refers to abundance of AMFspecies and suggest their coexistence by reduced competition betweenthem, enhancing ecosystem health.

ARBUSCULAR MYCORRHIZAL FUNGI AND HEAVY METALS

While many heavy metals (zinc, copper, cobalt, nickel, mercury, lead,cadmium, silver and chromo) (Berry and Wallace, 1981) haveconsiderable toxicity, others are essential micronutrients for animals,plants and many micro-organisms. It is known that most vascular plantsneed 17 essential elements for normal growth and development (seeRaven et al., 2005).

Certain elements that are normally toxic are, for certain organismsor under certain conditions, beneficial (vanadium, tungsten, andcadmium). It is known that most metallophytes plants belong to thefamilies Brassicaceae and Caryophyllaceae, which are known as non-mycorrhizal plants (de Mars and Boerner, 1996). However, some speciesin these families, e.g., Biscutella laevigata and Thlaspi spp., are ableto develop symbioses with AM species such as Glomus intraradices(Hildebrandt et al., 2007).

Alleviating heavy metal toxicity by AMF colonization can vary toa large extent, depending on the heavy metal, its concentration in thesoil, the fungal partner, and the conditions of plant growth (Hildebrandtet al., 2007). Plant tolerance can be enhanced by inoculation with specificAMF (Cicatelli et al., 2010; Lingua et al. 2008).


More recently, Cicatelli et al. (2012) showed the improvement ofpoplar growth associated with increased uptake of Cu and Zn wheninoculated with Glomus spp. (specially with Glomus mosseae) ascompared with non-mycorrhizal plants.

In Brazil, some of the studies dealing with heavy metals such asthose by Dr Siqueira (Cabral et al., 2010; Silva et al., 2006; Siqueiraet al., 2011) showed the retention capacity of Cu, Zn, Cd, and Pb byAMF mycelium, which differed amongst the different AMF species.Moreover, soil amendments for remediating metal contaminated soilin the tropics were indicated.

Dr Marta Cabello’s pioneer work conducted in hydrocarbons pollutedareas in Argentina, showed that native AMF, its isolation, quantificationof infectivity of indigenous propagules and its effectiveness could beapplied in bioremediation programs (Cabello, 1997, 2001). Her resultsconfirmed the beneficial effects of AMF as inoculants due to theincreased hosts efficient adaptation to contamination. Furthermore,those results suggested a huge importance of the selection of AMFspecies to be included in revegetation/restoration practices. A protocolfor studying the effect of hydrocarbon pollution on AM plants ispresented in Fig. 1.

It is known that the presence of gold and their exploration resultsin fine sulphidic, saline wastes (tailings), which contain toxic elementsand compounds such as cadmium, lead, manganese, cyanide, andparticularly arsenic. In Spain, for example, strong evidence that AMplants can develop arsenate resistance has been presented by González-Chávez et al. (2002).

In Brazil, Pagano et al. (2007) have studied differences in P responseof native Brazilian trees to inoculation with arbuscular mycorrhizalfungi. One of them, Anadenanthera peregrina Speg., has increasedpotential use in recuperation of degraded lands; however, the nutritionalrequirements are scarcely known and the AMF symbioses have beenshowed in greenhouse (Pereira et al., 1996; Carneiro et al., 1998; Pagano,2007). Pagano et al. (2007) have found that young Anadenantheraperegrina is AMF–independent, but a P-responsive species. In this way,P fertilizer should be applied in order to guarantee adequate seedlingdevelopment. Moreover, those authors showed that inoculation ofselected AMF species (Scutellospora heterogama) improved growthparameters and P concentration in leaves (Table 3). To know theresponse to fertilization and inoculation with AMF species of treesspecies is a very useful information. In the case of P, the competition


between arsenate (and As) and phosphate for adsorption sites in soilsand absorption by plants have been showed. Moreover it is known thatP addition to soil can increase phytotoxicity realizing more As for thesoil solution (Melo et al., 2007). This can be explained in terms ofsimilarity between As and P. Plants with high P doses also decreasedarsenate levels in nectar, even when subjected to high arsenate levels.Additionally, other reports suggest that the sequestration of As is notperformed in leaves, which will result in litter without As. Surprisingly,a recent report showed that A. peregrina did not tolerate As without

Fig. 1: Protocol for studying the effect of hydrocarbon pollution on AM plants. Rootsof plants growing in the polluted soils are stained for AM colonization (a).Determination of infective propagules including spores (b) and trap culturesagainst soil samples are required (Adapted from Cabello, 2001; Photos by M.Pagano).


the AMF symbiosis (Gomes et al., 2012). In this sense A. peregrinashowed great potential for phytoremediation, particularly for As (withtoxicity and potential risk to ecosystems as well as to human health)and abundant in contaminated sites (e.g. mining tailings in Minas GeraisState, Brazil). Given the potential benefits to environment of A.peregrina, it is not surprising that manipulation of AMF communitiesneeds to be more carefully investigated.

Moreover, AMF inoculation can reduce the uptake of HM and arsenicfrom metal contaminated biosolids and tailings and thus diminish therisk for the food chain. However, it will depend on the part of the plantthat accumulates the HM and the part that is use for food. The nativelegume species A. peregrina also showed tolerance to E. camaldulensisand E. grandis oils, being tested, in field conditions, inoculated (AMFand rhizobia) and mixed with E. camaldulensis plants (Duarte et al.,2012). In this sense it is known that the production of allelochemicalsis regulated by diverse factors (environmental: temperature, lightintensity, water and nutrient availability, soil texture and micro-organisms) (Chou and Kuo, 1986; Carmo et al., 2007). Furthermore,factors related to stress can increase their biologic activity (Rizvi andRizvi 1992; Einhellig, 1999; Inderjit et al. 2006). Once more we detectedAMF, and also ectomycorrhiza, in plants of E. camaldulensis(monoculture and mixed plantations) (Pagano and Scotti, 2008).

Table 3: Response of A. peregrina to AMF inoculation and P fertilization 150 daysafter sowing. Values followed by the same letter in each column do not differsignificantly by One way ANOVA and Tukey´s HSD test p<0.05. Adaptedfrom Pagano et al. (2007).

AMF inoculation P fertilization Plant height P concentration in(cm) leaves (mg g–1)

Glomus 32.5 mg dm–3 16.5a 1.15a

65 mg dm–3 24.0b 1.82a

136 mg dm–3 17.1a 1.92a

Gigaspora 32.5 mg dm–3 16.5a 1.36a

65 mg dm–3 14.3a 1.63a

136 mg dm–3 28.1ab 2.84ab

Scutellospora 32.5 mg dm–3 13.5a 1.14a

65 mg dm–3 14.5a 1.33a

136 mg dm–3 33.6b 4.00b

Acaulospora 32.5 mg dm–3 12.3a 0.99a

65 mg dm–3 20.9b 2.29a

136 mg dm–3 25.6ab 1.98a

Non inoculated 136 mg dm–3 32.1ab 2.73ab


BIOCHAR STIMULATION OF BENEFICIAL SOIL MICROBIOTA

Given the potential benefits to agricultural productivity, biochar soilamendment not only can contribute to improved soil fertility, but canbenefit microorganism populations that promote plant growth andresistance to biotic stresses (soil borne diseases and foliar pathogens).However, the mechanisms by which it is beneficial are scarcelyunderstood, as well as the indirect effects (increased water and nutrientretention, improvements in soil pH, increased soil cation exchangecapacity, effects on P and S transformations, neutralization of phytotoxiccompounds, improved soil physical properties, and alteration of soilmicrobiota (Elad et al., 2011)). Interestingly, biochar promote AMF andin this regard, further studies are needed (Warnock et al., 2007). Itmust be stressed that there is much future research to elucidate the“Biochar Effect” (Elad et al., 2011). Recent studies, for example, showedthat biochar addition to asparagus field soil resulted in reductions inroot lesions caused by Fusarium sp. compared with a non-amendedcontrol (Elmer and Pignatello, 2011). Moreover, biochar amendmentsimproved AM colonization of asparagus roots, contributing to controldiseases (Elmer and Pignatello, 2011). It is also known that biocharmay help to remove allelopathic effects via adsorption and detoxification,as pointed by Wardle et al. (1998).

Further studies evaluating the types of biochar (depending on originalfeedstock and pyrolysis conditions) (Downie et al., 2009; Krull et al.,2009) that induce resistance responses in plants against a broad rangeof pathogens and parasites including fungi, bacteria, viruses andnematodes, are urgently needed.

CONCLUSION

In the introduction to this chapter, we briefly described plant stressfactors and the benefits that mycorrhizal fungi provide to their planthosts.

Throughout the chapter, we have showed that stress affects soilphysical and chemical properties, influencing the population, diversityand activities of soil microbes, including symbiotic fungal populations.To know the mycotrophic status of plant species is essential, and droughtstress increasingly link plant to soil. Additionally, flooding andanthropogenic alterations (tillage) were discussed although the lackof more detailed studies.


The alleviation of heavy metal stress would have great implicationin the manipulation of AMF species able to colonize plants in pollutedsoils approving the potential of AMF to be incorporated inphytoextraction technologies as mycorrhizo remediation.

This chapter argues that AMF alleviate biotic stresses which havegreater effect on plant growth than increasing the amount of pesticidesor fertilizer commonly added; however, to develop technologies andprotocols are crucial. Consequently, further research is needed to copeplant stresses.

Finally, as cattle and agriculture are increasing activities, thepotential benefits to agricultural productivity of biochar soil amendmentand their interactions with mycorrhizal plants were also pointed.

ACKNOWLEDGEMENTS

M. Pagano is grateful to the Council for the Development of HigherEducation at Graduate Level, Brazil (CAPES), and to the Minas GeraisState Agency for Research and Development (FAPEMIG) for thepostdoctoral scholarships granted. M.N. Cabello is a researcher fromComisión de Investigaciones Científicas (CIC) Provincia Bs. As.,Argentina.

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